Primary and secondary motoneurons use different calcium channel types to control escape and swimming behaviors in zebrafish

Abstract

The escape response and rhythmic swimming in zebrafish are distinct behaviors mediated by two functionally distinct motoneuron (Mn) types. The primary (1°Mn) type depresses and has a large quantal content (Qc) and a high release probability (Pr). Conversely, the secondary (2°Mn) type facilitates and has low and variable Qc and Pr. This functional duality matches well the distinct associated behaviors, with the 1°Mn providing the strong, singular C bend initiating escape and the 2°Mn conferring weaker, rhythmic contractions. Contributing to these functional distinctions is our identification of P/Q-type calcium channels mediating transmitter release in 1°Mns and N-type channels in 2°Mns. Remarkably, despite these functional and behavioral distinctions, all ∼15 individual synapses on each muscle cell are shared by a 1°Mn bouton and at least one 2°Mn bouton. This blueprint of synaptic sharing provides an efficient way of controlling two different behaviors at the level of a single postsynaptic cell.

Long-Term Exposure to SSRI Citalopram Induces Neurotoxic Effects in Zebrafish

“…F1 + larvae in the 100 μg/L citalopram exposure group did not display detectable differences in the length of the axon bundle interval (Figure b; P > 0.05) but did show significantly shorter spinal MN projections (Figure c; P = 0.0382) than those of the controls. Moreover, the aberrant morphological features of spinal motor axons described in this study are known to affect the motor behavior of zebrafish larvae . The neurotoxic effects of some environmental contaminants (such as titanium dioxide nanoparticles and chlorpyrifos-oxon) on the development of zebrafish spinal MNs have been documented.…”

“…Moreover, the aberrant morphological features of spinal motor axons described in this study are known to affect the motor behavior of zebrafish larvae. 44 The neurotoxic effects of some environmental contaminants (such as titanium dioxide nanoparticles 45 and chlorpyrifos-oxon 46 ) on the development of zebrafish spinal MNs have been documented. Similarly, the inhibited growth of spinal MNs in this study suggests that motor axons may be the primary targets of citalopram and that these spinal MN defects may decrease motor performance in larvae.…”

The Temporal Mechanisms Guiding Interneuron Differentiation in the Spinal Cord

“…Primary MNs have larger soma sizes, smaller input resistances, more extensive dendritic branching, larger axon diameters and more ventromedial axon projection pathways and settle within relatively more dorsal positions than secondary MNs [ 59 , 60 , 61 ]. Primary and secondary MNs also express distinct calcium channel types, resulting in distinct neurotransmitter release properties and downstream muscle fibre control [ 62 ]. Thus, neurogenesis timing appears to serve as an early organizing principle for the anatomical and intrinsic properties of zebrafish MNs, resulting in fast and slow swimming control.…”

“…Small amplitude (Amp) and low frequency swimming emerge later, at 4–5 days post feralization (dpf), in the zebrafish larvae ( B ) [ 48 , 49 ]. Early maturation of swimming behaviours is underscored by sequential waves of neurogenesis ( C ), early-born and fast swimming recruitment; ( D ), late-born and slow swimming recruitment; motor neurons (MNs), [ 49 ]; V0, [ 48 , 49 , 55 ]; V2a INs, [ 52 ]; V1 INs, [ 53 ]; dI6 INs, [ 62 ]. Neurogenesis time- and speed-matched spinal IN subclasses display distinct circuit connectivities.…”

“…Thus, further subpopulation heterogeneity exists within the late-born neurogenesis window of V0-e INs. Although MCoD INs were specifically recruited during slower swimming speeds in the larvae zebrafish [ 48 , 49 ], no correlation between morphology and speed-dependent recruitment of V0-e INs was found in the adult spinal cord [ 62 ]. Therefore, it is possible that either early morphological distinctions in the larvae are lost in the adult, or that V0-e IN recruitment patterns change with maturation.…”